Single article

DOI: 10.47026/2413-4864-2024-1-74-81
Full article

UDC: 611.013.11
BBC: 51.161.10

Belyaeva L.A., Shurygina O.V., Zhilkina M.P., Mironov S.Yu., Kulakova O.V., Bovtunova S.S., Shurygina A.S.

Hyperactivation of Spermatozoa and its Role in the Fertilization Process

Keywords: spermatozoid, hyperactivation, infertility, fertilization

To date, according to the WHO estimates, every sixth person in the world faces the problem of infertility, while the contribution of the male factor is, according to various sources, from 30 to 50%. Understanding the cellular and molecular processes that lead to spermatozoa motility is necessary for accurate diagnosis and finding solutions to this problem. The purpose of the review is to analyze and evaluate current data on the problem of spermatozoa hyperactivation, the causes of its violation, molecular mechanisms and prognostic value. Materials and methods. Domestic and foreign sources of literature dated from 1987 to 2022 were used, they were taken from electronic libraries of scientific publications and medical databases, in particular "CyberLeninka", "Google Academy", "ScienceResearch", Elibrary.ru and PubMed. The review included the sources relevant to the topic of this review, which were searched using keywords such as spermatozoid, hyperactivation, infertility, fertilization. Research results. Hyperactivation of spermatozoa is one of the factors that ensure fertilization. This is a Ca2+ and energy-dependent process due to the normal operation of CatSper and KSper channels, as well as cAMP-, cGMP-dependent, potential-dependent channels. In the absence of the SLC9A10 gene in male mice, spermatozoa mature immobile, despite satisfactory spermatogenesis. The control units in the sperm flagella, consisting of CatSper, SLC9A10 and ABHD2, located on the surface, are necessary to ensure rapid signal transmission and coordinated control of complex cellular movement (hyperactivation and rotation). Conclusions. The motility of spermatozoa acquired during their hyperactivation is a vital functional characteristic that determines the ability of male germ cells to penetrate and migrate both into the cervical mucus and into the oocyte membrane (and ultimately fertilize it). Violation of hyperactivation processes or its absence can result in fertilization failure and, in consequence of, be one of the causes of infertility in a couple.

References

  1. Alvarez L., Friedrich B.M., Gompper G. et al. The computational sperm cell. Cell. Biol., 2014, vol. 24(3), pp. 198–207. DOI:10.1016/j.tcb.2013.10.004.
  2. Arcelay E., Salicioni A.M., Wertheimer E. et al. Identification of proteins undergoing tyrosine phosphorylation during mouse sperm capacitation. J. Dev. Biol., 2008, vol. 52(5-6), pp. 463–472. DOI: 10.1387/ijdb.072555ea.
  3. Armon L., Eisenbach M. Behavioral mechanism during human sperm chemotaxis: involvement of hyperactivation. PLoS One, 2011, vol. 6(12), p. e28359. DOI: 10.1371/journal.pone.0028359.
  4. Bastiaan H., Franken D. The influence of homogenous zona pellucida on human spermatozoa hyperactivation, acrosome reaction and zona binding. Andrologia, 2007, vol. 39(1), pp. 7–11. DOI: 10.1111/j.1439-0272.2006.00751.x.
  5. Berendsen J.T.W., Kruit S.A., Atak N. et al. Flow-Free Microfluidic Device for Quantifying Chemotaxis in Spermatozoa. Chem., 2020, vol. 92(4), pp. 3302–3306. DOI: 10.1021/acs.analchem.9b05183p.
  6. Björndahl L., Barratt C.L.R., Mortimer D. et al. Standards in semen examination: publishing reproducible and reliable date based on high-quality methodology. Reprod., 2022, vol. 37(11), pp. 2497–2502. DOI: 10.1093/humrep/deac189.PMID: 36112046.
  7. Carlson A.E., Westenbroek R.E., Quill T. et al. CatSper1 required for evoked Ca2+ entry and control of flagellar function in sperm. Natl. Acad. Sci. USA, 2003, vol. 100(25), pp. 14864–14868. DOI: 10.1073/pnas.2536658100.
  8. Cohen-Dayag A., Ralt D., Tur-Kaspa I. et al. Sequential acquisition of chemotactic responsiveness by human spermatozoa. Reprod., 1994, vol. 50(4), pp. 786–790. DOI: 10.1095/biolreprod50.4.786.
  9. De La Vega-Beltran J.L., Sánchez-Cárdenas C., Krapf D. et al. Mouse sperm membrane potential hyperpolarization is necessary and sufficient to prepare sperm for the acrosome reaction. Biol. Chem., 2012, vol. 287(53), pp. 44384–44393. DOI: 10.1074/jbc.M112.393488.
  10. Finkelstein M., Etkovitz N., Breitbart H. Ca2+ signaling in mammalian spermatozoa. Cell. Endocrinol., 2020, vol. 516, p. 110953. DOI: 10.1016/j.mce.2020.110953.
  11. Hansen J.N., Rassmann S., Jikeli J.F. et al. SpermQ-a Simple Analysis Software to Comprehensively Study Flagellar Beating and Sperm Steering. , 2018, vol. 8(1), p. 10. DOI: 10.3390/cells8010010.
  12. Hermes G.H., Herrera P.H., Montoya F. et al. Human sperm uses asymmetric and anisotropic flagellar controls to regulate swimming symmetry and cell steering. Science Advances, 2020, vol. 6(31), eaba5168. DOI: 10.1126/sciadv.aba5168.
  13. Ho H.C., Granish K.A., Suarez S.S. Hyperactivated motility of bull sperm is triggered at the axoneme by Ca2+ and not cAMP. Biol., 2002, vol. 250(1), pp. 208–217. DOI: 10.1006/dbio.2002.0797.
  14. Hunter R.H., Nichol R. A preovulatory temperature gradient between the isthmus and ampulla of pig oviducts during the phase of sperm storage. Reprod. Fertil., 1986, vol. 77(2), pp. 599–606. DOI: 10.1530/jrf.0.0770599.
  15. Ishijima S., Mohri H., Overstreet J.W. et al. Hyperactivation of monkey spermatozoa is triggered by Ca2+ and completed by cAMP. Reprod. Dev., 2006, vol. 73(9), pp. 1129–1139. DOI: 10.1002/mrd.20420.
  16. Krapf D., Arcelay E., Wertheimer E.V. et al. Inhibition of Ser/Thr phosphatases induces capacitation-associated signaling in the presence of Src kinase inhibitors. Biol. Chem., 2010, vol. 285(11), pp. 7977–7985. DOI: 10.1074/jbc.M109.085845.
  17. Miller M.R., Kenny S.J., Mannowetz N. et al. Asymmetrically Positioned Flagellar Control Units Regulate Human Sperm Rotation. Rep., 2018, vol. 24(10), pp. 2606–2613. DOI: 10.1016/j.celrep.2018.08.016.
  18. Miller M.R., Mannowetz N., Iavarone A.T. et al. Unconventional endocannabinoid signaling governs sperm activation via the sex hormone progesterone. Science, 2016, vol. 352(6285), pp. 555–559. DOI:10.1126/science.aad6887.
  19. Minhas S., Bettocchi C., Boeri L. et al. EAU Working Group on Male Sexual and Reproductive Health. European Association of Urology Guidelines on Male Sexual and Reproductive Health, 2021, Update on Male Infertility. Eur., 2021, vol. 80(5), pp. 603–620. DOI: 10.1016/j.eururo.2021.08.014.
  20. Mortimer S.T., van der Horst G., Mortimer D. The future of computer sperm-aided sperm analysis. Asian J. Androl., 2015, vol. 17(4), pp. 545–553. DOI: 10.4103/1008-682X.154312.
  21. Smith D.J., Gaffney E.A., Gadêlha H. et al. Bend propagation in the flagella of migrating human sperm, and its modulation by viscosity. Motil. Cytoskeleton, 2009, vol. 66(4), pp. 220–236. DOI: 10.1002/cm.20345.
  22. Spehr M., Schwane K., Riffell J.A. et al. Particulate adenylate cyclase plays a key role in human sperm olfactory receptor-mediated chemotaxis. Biol. Chem., 2004, vol. 279(38), pp. 40194–40203. DOI: 10.1074/jbc.M403913200.
  23. Stival C., Puga Molina L. del C., Paudel B. et al. Sperm Capacitation and Acrosome Reaction in Mammalian Sperm. Anat. Embryol. Cell. Biol., 2016, vol. 220, pp. 93–106. DOI: 10.1007/978-3-319-30567-7_5.
  24. Van der Horst G. Status of Sperm Functionality Assessment in Wildlife Species: From Fish to Primates. Animals (Basel), 2021, vol. 11(6), p. 1491. DOI: 10.3390/ani11061491.
  25. Van der Horst G., Bennett M., Bishop J.D.D. CASA in invertebrates. Fertil. Dev., 2018, vol. 30(6), pp. 907–918. DOI: 10.1071/RD17470.
  26. Van der Horst G., Maree L. Origin, migration and reproduction of indigenous domestic animals with special reference to their sperm quality. Animals (Basel), 2022, Mar. 5, vol. 12(5), p. 657. DOI: 10.3390/ani12050657.PMID: 35268225.
  27. Van der Horst G., Maree L. Sperm form and function in the absence of sperm competition. Reprod. Dev., 2014, Mar., vol. 81(3), pp. 204–216. DOI: 10.1002/mrd.22277.
  28. Visconti P.E., Moore G.D., Bailey J.L. et al. Capacitation of mouse spermatozoa. II. Protein tyrosine phosphorylation and capacitation are regulated by a cAMP-dependent pathway. Development., 1995, vol. 121(4), pp. 1139–1150. DOI: 10.1242/dev.121.4.1139.
  29. Wang D., Hu J., Bobulescu I.A. et al. A sperm-specific Na+/H+ exchanger (sNHE) is critical for expression and in vivo bicarbonate regulation of the soluble adenylyl cyclase (sAC). Natl. Acad. Sci. USA, 2007, vol. 104(22), pp. 9325–9330. DOI: 10.1073/pnas.0611296104.
  30. Wang D., King S.M., Quill T.A. et al. A new sperm-specific Na+/H+ exchanger required for sperm motility and fertility. Cell. Biol., 2003, vol. 5(12), pp. 1117–1122. DOI: 10.1038/ncb1072.
  31. Yanagimachi R. In vitro capacitation of hamster spermatozoa by follicular fluid. Reprod. Fertil., 1969, vol. 18(2), pp. 275–286. DOI: 10.1530/jrf.0.0180275.
  32. Zeng X.H., Yang C., Kim S.T. et al. Deletion of the Slo3 gene abolishes alkalization-activated K+ current in mouse spermatozoa. Natl. Acad. Sci. USA, 2011, vol. 108(14), pp. 5879–5884. DOI: 10.1073/pnas.1100240108.

About authors

Belyaeva Lidiya A.
Post-Graduate Student, Department of Histology and Embryology, Samara State Medical University, Russia, Samara (llibel@mail.ru; ORCID: https://orcid.org/0000-0003-2095-0452)
Shurygina Oksana V.
Doctor of Medical Sciences, Professor, Department of Histology and Embryology, Department of Reproductive Medicine, Clinical Embryology and Genetics, Samara State Medical University; Head of the Embryological Laboratory, Clinical Hospital IDK "Mother and Child", Russia, Samara (oks-shurygina@yandex.ru; ORCID: https://orcid.org/0000-0002-3903-4350)
Zhilkina Maria P.
4th year Student, Institute of Clinical Medicine, Samara State Medical University, Russia, Samara (jilkina.masha@yandex.ru; )
Mironov Sergey Yu.
a Competitor of Scientific Degree of Candidate of Medical Sciences Science, Department of Histology and Embryology, Samara State Medical University, Russia, Samara (mironov0511@mail.ru; ORCID: https://orcid.org/0000-0002-9291-5376)
Kulakova Olesya V.
Candidate of Medical Sciences, Associate Professor, Department of Histology and Embryology, Samara State Medical University, Russia, Samara (olesvk@mail.ru; ORCID: https://orcid.org/0000-0002-8318-0355)
Bovtunova Svetlana S.
Candidate of Medical Sciences, Associate Professor, Department of Histology and Embryology, Samara State Medical University, Russia, Samara (s.s.bovtunova@samsmu.ru; ORCID: https://orcid.org/0000-0003-4920-2511)
Shurygina Alina S.
3rd year Student, Institute of Clinical Medicine, Samara State Medical University, Russia, Samara (Al.shurygina@yandex.ru; ORCID: https://orcid.org/0009-0004-8923-6446)

Article link

Belyaeva L.A., Shurygina O.V., Zhilkina M.P., Mironov S.Yu., Kulakova O.V., Bovtunova S.S., Shurygina A.S. Hyperactivation of Spermatozoa and its Role in the Fertilization Process [Electronic resource] // Acta medica Eurasica. – 2024. – №1. P. 74-81. – URL: https://acta-medica-eurasica.ru/en/single/2024/1/8/. DOI: 10.47026/2413-4864-2024-1-74-81.

Menu

Journal numbers

Archive for year 2024
Archive for year 2023
Archive for year 2022
Archive for year 2021
Archive for year 2020
Archive for year 2019
Archive for year 2018
Archive for year 2017
Archive for year 2016
Archive for year 2015